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Monaghan was born in Santa Monica, California, the only child of Diane Monaghan, an insurance claims specialist and single mother. He and his mother relocated to Boca Raton, Florida, shortly after his birth. Recognizing that Monaghan was an exceptionally outgoing child, his mother sent his picture to modeling agencies when he was three. He appeared on the cover of his first catalogue at the age of five and appeared in his first regional commercial at seven.[2][3]

Monaghan first came to national attention in 2003 for his role as Winthrop Paroo opposite Kristin Chenoweth and Matthew Broderick in the ABC television adaptation of The Music Man. When recounting the decision to cast the 9-year-old Monaghan, director and executive-producer Jeff Bleckner explained, "There are some people, when you put them up on film, they sort of pop off the screen at you. That's how it was with Cameron. From the second we saw him, he was it. We were looking for anybody who had that wonderful appeal. And Cameron had it."[2]

In April 2010, Monaghan was cast as an ensemble cast member on the Showtime comedy-drama series Shameless.[6] On the series, which premiered in January 2011, Monaghan portrays Ian Gallagher, the gaybipolar teenage son of a large dysfunctional Chicago family. Sarah Hughes of The Independent commended Monaghan's portrayal for providing "one of the more nuanced depictions of a gay teenager to be seen on US TV."[7] Matthew Gilbert of The Boston Globe described Monaghan's performance as "extraordinary."[8] And the gay-interest media outlet AfterElton.com cited Monaghan's portrayal of Ian in naming him to its list of "2011's Break-Out TV Actors".[9] In February 2014, Showtime announced it had renewed the series for a fifth season, scheduled to begin airing in 2015.[10] For his work in the fifth season, Monaghan received a Critic's Choice Award nomination for Best Supporting Actor in a Comedy Series. The seventh season began airing in October 2016. The eighth season, consisting of 12 episodes, went into production in May 2017; it premiered on November 5, 2017.[citation needed] The series was renewed for a ninth season which premiered on September 9, 2018.[11] Monaghan announced via Instagram that he would be leaving the series following the sixth episode of the ninth season.[12]

In addition to his role on Shameless, Monaghan has continued to appear in a variety of episodic television roles. In 2011, he guest-starred as Nick Peyton, a teenage boy accused of murdering his Marine father, on the CBS crime series NCIS. That same year he appeared as Jonathan McKenna on the TNT mystery series Rizzoli & Isles. In 2012, he guest-starred as Eddie Sandow, a 19-year-old who creates a hostage situation after his father is accused of sexual assault, on the NBC crime series Law & Order: Special Victims Unit.[5]

In addition to his television credits, Monaghan has continued to appear in a variety of feature film roles. In 2011, he co-starred as high school sophomore Corey Doyle in the Disney teen drama Prom. In 2012, he portrayed Jake, the son of an attractive YMCA director in the sports themed comedy 2nd Serve. In 2014, Monaghan starred as Adam McCormick, a small-town high school athlete who becomes consumed by the death of one of his classmates in the independent drama Jamie Marks Is Dead. That same year, he appeared as Mason Ashford, the best friend and romantic interest to Rose in the fantasy adventure film Vampire Academy.[5][13][14] He also starred as Asher in the dystopian movie The Giver, alongside Brenton Thwaites, Odeya Rush, Jeff Bridges and Meryl Streep.

Since 2015, he has appeared in the television series Gotham as Jerome Valeska, a character similar to the Joker, the archenemy of Batman. Starting in 2018, he was revealed to also be playing Jeremiah Valeska, the character's twin brother.